Decoupling speciation and extinction reveals both abiotic and biotic drivers shaped 250 million years of diversity in crocodile-line archosaurs.

Whereas living representatives of Pseudosuchia, crocodylians, number fewer than 30 species, more than 700 pseudosuchian species are known from their 250-million-year fossil record, displaying far greater ecomorphological diversity than their extant counterparts. With a new time-calibrated tree of >500 species, we use a phylogenetic framework to reveal that pseudosuchian evolutionary history and diversification dynamics were directly shaped by the interplay of abiotic and biotic processes over hundreds of millions of years, supported by information theory analyses. Speciation, but not extinction, is correlated with higher temperatures in terrestrial and marine lineages, with high sea level associated with heightened extinction in non-marine taxa. Low lineage diversity and increased speciation in non-marine species is consistent with opportunities for niche-filling, whereas increased competition may have led to elevated extinction rates. In marine lineages, competition via increased lineage diversity appears to have driven both speciation and extinction. Decoupling speciation and extinction, in combination with ecological partitioning, reveals a more complex picture of pseudosuchian evolution than previously understood. As the number of species threatened with extinction by anthropogenic climate change continues to rise, the fossil record provides a unique window into the drivers that led to clade success and those that may ultimately lead to extinction.

Speciation across the Earth driven by global cooling in terrestrial orchids.

Although climate change has been implicated as a major catalyst of diversification, its effects are thought to be inconsistent and much less pervasive than localized climate or the accumulation of species with time. Focused analyses of highly speciose clades are needed in order to disentangle the consequences of climate change, geography, and time. Here, we show that global cooling shapes the biodiversity of terrestrial orchids. Using a phylogeny of 1,475 species of Orchidoideae, the largest terrestrial orchid subfamily, we find that speciation rate is dependent on historic global cooling, not time, tropical distributions, elevation, variation in chromosome number, or other types of historic climate change. Relative to the gradual accumulation of species with time, models specifying speciation driven by historic global cooling are over 700 times more likely. Evidence ratios estimated for 212 other plant and animal groups reveal that terrestrial orchids represent one of the best-supported cases of temperature-spurred speciation yet reported. Employing >2.5 million georeferenced records, we find that global cooling drove contemporaneous diversification in each of the seven major orchid bioregions of the Earth. With current emphasis on understanding and predicting the immediate impacts of global warming, our study provides a clear case study of the long-term impacts of global climate change on biodiversity.

Lost, gained, and regained functional and phylogenetic diversity of European mammals since 8000 years ago.

Mammals have experienced high levels of human-mediated extirpations but have also been widely introduced to new locations, and some have recovered from historic persecution. Both of these processes-losses and gains-have resulted in concern about functional losses and changes in ecological communities as new ecological states develop. The question of whether species turnover inevitably leads to declines in functional and phylogenetic diversity depends, however, on the traits and phylogenetic distinctiveness of the species that are lost, gained, or regained. Comparing ~8000 years ago with the last century, we show that extirpations and range retractions have indeed reduced the functional and phylogenetic diversity of mammals in most European regions (countries and island groups), but species recoveries and the introduction of non-native species have increased functional and phylogenetic diversity by equivalent or greater amounts in many regions. Overall, across Europe, species richness increased in 41 regions over the last 8000 years and declined in 1; phylogenetic diversity increased in 33 and declined in 12, while functional diversity results showed 20 increases and 25 decreases. The balance of losses (extirpations) and gains (introductions, range expansions) has, however, led to net increases in functional diversity on many islands, where the original diversity was low, and across most of western Europe. Historically extirpated mega- and mesofaunal species have recolonized or been reintroduced to many European regions, contributing to recent functional and phylogenetic diversity recovery. If conservation rewilding projects continue to reintroduce regionally extirpated species and domestic descendants of "extinct" species to provide replacement grazing, browsing, and predation, there is potential to generate net functional and phylogenetic diversity gains (relative to 8000 years ago) in most European regions.

Ecological Transitions and the Shape of the Decapod Tree of Life.

Understanding the processes that shaped the distribution of species richness across the Tree of Life is a central macroevolutionary research agenda. Major ecological innovations, including transitions between habitats, may help to explain the striking asymmetries of diversity that are often observed between sister clades. Here, we test the impact of such transitions on speciation rates across decapod crustaceans, modeling diversification dynamics within a phylogenetic framework. Our results show that, while terrestrial lineages have higher speciation rates than either marine or freshwater lineages, there is no difference between mean speciation rates in marine and freshwater lineages across Decapoda. Partitioning our data by infraorder reveals that those clades with habitat heterogeneity have higher speciation rates in freshwater and terrestrial lineages, with freshwater rates up to 1.5 times faster than marine rates, and terrestrial rates approximately four times faster. This averaging out of marine and freshwater speciation rates results from the varying contributions of different clades to average speciation rates. However, with the exception of Caridea, we find no evidence for any causal relationship between habitat and speciation rate. Our results demonstrate that while statistical generalizations about ecological traits and evolutionary rates are valuable, there are many exceptions. Hence, while freshwater and terrestrial lineages typically speciate faster than their marine relatives, there are many atypically slow freshwater lineages and fast marine lineages across Decapoda. Future work on diversification patterns will benefit from the inclusion of fossil data, as well as additional ecological factors.

Disparities in the analysis of morphological disparity.

Analyses of morphological disparity have been used to characterize and investigate the evolution of variation in the anatomy, function and ecology of organisms since the 1980s. While a diversity of methods have been employed, it is unclear whether they provide equivalent insights. Here, we review the most commonly used approaches for characterizing and analysing morphological disparity, all of which have associated limitations that, if ignored, can lead to misinterpretation. We propose best practice guidelines for disparity analyses, while noting that there can be no 'one-size-fits-all' approach. The available tools should always be used in the context of a specific biological question that will determine data and method selection at every stage of the analysis.

Comparing Life Histories across Taxonomic Groups in Multiple Dimensions: How Mammal-Like Are Insects?

Explaining variation in life histories remains a major challenge because they are multidimensional and there are many competing explanatory theories and paradigms. An influential concept in life-history theory is the fast-slow continuum, exemplified by mammals. Determining the utility of such concepts across taxonomic groups requires comparison of the groups' life histories in multidimensional space. Insects display enormous species richness and phenotypic diversity, but testing hypotheses like the fast-slow continuum has been inhibited by incomplete trait data. We use phylogenetic imputation to generate complete data sets of seven life-history traits in orthopterans (grasshoppers and crickets) and examine the robustness of these imputations for our findings. Three phylogenetic principal components explain 83%-96% of variation in these data. We find consistent evidence of an axis mostly following expectations of a fast-slow continuum, except that "slow" species produce larger, not smaller, clutches of eggs. We show that the principal axes of variation in orthopterans and reptiles are mutually explanatory, as are those of mammals and birds. Essentially, trait covariation in Orthoptera, with "slow" species producing larger clutches, is more reptilelike than mammal-like or birdlike. We conclude that the fast-slow continuum is less pronounced in Orthoptera than it is in birds and mammals, reducing the universal relevance of this pattern and the theories that predict it.

Phylogenetic supertree and functional trait database for all extant parrots.

We present a complete dataset from the literature on functional traits including morphological measurements, dietary information, foraging strategy, and foraging location for all 398 extant species of parrots. The morphological measurements include: mass, total length, wing chord, culmen length, tarsus length, and tail length. The diet data describe whether each species is known to consume particular food items (e.g. nectar, berries, and carrion), foraging strategy data describes how each species captures or accesses food, and foraging location data describe the habitat from which each species finds food (e.g. ground, canopy, and subcanopy). We also present a time-calibrated phylogenetic supertree that contains all 398 extant species as well as 15 extinct species (413 total species). These data are hosted on the Figshare data depository (https://figshare.com/s/6cdf8cf00793deab7ba6).

Elevated atmospheric CO2 promoted speciation in mosquitoes (Diptera, Culicidae).

Mosquitoes are of great medical significance as vectors of deadly diseases. Despite this, little is known about their evolutionary history or how their present day diversity has been shaped. Within a phylogenetic framework, here we show a strong correlation between climate change and mosquito speciation rates: the first time to our knowledge such an effect has been demonstrated for insects. Information theory reveals that although climate change is correlated with mosquito evolution there are other important factors at play. We identify one such driver to be the rise of mammals, which are predominant hosts of Culicidae. Regardless of the precise mechanism, we demonstrate a strong historical association. This finding, taken in combination with projected rises in atmospheric CO2 from anthropogenic activity, has important implications for culicid vector distributions and abundance, and consequently for human health.

Freshwater transitions and symbioses shaped the evolution and extant diversity of caridean shrimps.

Understanding the processes that shaped the strikingly irregular distribution of species richness across the Tree of Life is a major research agenda. Changes in ecology may go some way to explain the often strongly asymmetrical fates of sister clades, and we test this in the caridean shrimps. First appearing in the Lower Jurassic, there are now ~3500 species worldwide. Carideans experienced several independent transitions to freshwater from marine habitats, while many of the marine species have also evolved a symbiotic lifestyle. Here we use diversification rate analyses to test whether these ecological traits promote or inhibit diversity within a phylogenetic framework. We demonstrate that speciation rates are more than twice as high in freshwater clades, whilst symbiotic ecologies are associated with lower speciation rates. These lower rates amongst symbiotic species are of concern given that symbioses often occur in some of the most diverse, delicately balanced and threatened marine ecosystems.

Global cooling as a driver of diversification in a major marine clade.

Climate is a strong driver of global diversity and will become increasingly important as human influences drive temperature changes at unprecedented rates. Here we investigate diversification and speciation trends within a diverse group of aquatic crustaceans, the Anomura. We use a phylogenetic framework to demonstrate that speciation rate is correlated with global cooling across the entire tree, in contrast to previous studies. Additionally, we find that marine clades continue to show evidence of increased speciation rates with cooler global temperatures, while the single freshwater clade shows the opposite trend with speciation rates positively correlated to global warming. Our findings suggest that both global cooling and warming lead to diversification and that habitat plays a role in the responses of species to climate change. These results have important implications for our understanding of how extant biota respond to ongoing climate change and are of particular importance for conservation planning of marine ecosystems.

Towards a Supertree of Arthropoda: A Species-Level Supertree of the Spiny, Slipper and Coral Lobsters (Decapoda: Achelata).

While supertrees have been built for many vertebrate groups (notably birds, mammals and dinosaurs), invertebrates have attracted relatively little attention. The paucity of supertrees of arthropods is particularly surprising given their economic and ecological importance, as well as their overwhelming contribution to biodiversity. The absence of comprehensive archives of machine-readable source trees, coupled with the need for software implementing repeatable protocols for managing them, has undoubtedly impeded progress. Here we present a supertree of Achelata (spiny, slipper and coral lobsters) as a proof of concept, constructed using new supertree specific software (the Supertree Toolkit; STK) and following a published protocol. We also introduce a new resource for archiving and managing published source trees. Our supertree of Achelata is synthesised from morphological and molecular source trees, and represents the most complete species-level tree of the group to date. Our findings are consistent with recent taxonomic treatments, confirming the validity of just two families: Palinuridae and Scyllaridae; Synaxidae were resolved within Palinuridae. Monophyletic Silentes and Stridentes lineages are recovered within Palinuridae, and all sub-families within Scyllaridae are found to be monophyletic with the exception of Ibacinae. We demonstrate the feasibility of building larger supertrees of arthropods, with the ultimate objective of building a complete species-level phylogeny for the entire phylum using a divide and conquer strategy.

The Supertree Toolkit 2: a new and improved software package with a Graphical User Interface for supertree construction.

Building large supertrees involves the collection, storage, and processing of thousands of individual phylogenies to create large phylogenies with thousands to tens of thousands of taxa. Such large phylogenies are useful for macroevolutionary studies, comparative biology and in conservation and biodiversity. No easy to use and fully integrated software package currently exists to carry out this task. Here, we present a new Python-based software package that uses well defined XML schema to manage both data and metadata. It builds on previous versions by 1) including new processing steps, such as Safe Taxonomic Reduction, 2) using a user-friendly GUI that guides the user to complete at least the minimum information required and includes context-sensitive documentation, and 3) a revised storage format that integrates both tree- and meta-data into a single file. These data can then be manipulated according to a well-defined, but flexible, processing pipeline using either the GUI or a command-line based tool. Processing steps include standardising names, deleting or replacing taxa, ensuring adequate taxonomic overlap, ensuring data independence, and safe taxonomic reduction. This software has been successfully used to store and process data consisting of over 1000 trees ready for analyses using standard supertree methods. This software makes large supertree creation a much easier task and provides far greater flexibility for further work.

Reweaving the tapestry: a supertree of birds.

Our knowledge of the avian tree of life remains uncertain, particularly at deeper levels due to the rapid diversification early in their evolutionary history. They are the most abundant land vertebrate on the planet and have been of great historical interest to systematists. Birds are also economically and ecologically important and as a result are intensively studied, yet despite their importance and interest to humans around 13% of taxa currently on the endangered species list perhaps as a result of human activity. Despite all this no comprehensive phylogeny that includes both extinct and extant species currently exists. Here we present a species-level supertree, constructed using the Matrix Representation with Parsimony method, of Aves containing approximately two thirds of all species from nearly 1000 source phylogenies with a broad taxonomic coverage. The source data for the tree were collected and processed according to a strict protocol to ensure robust and accurate data handling. The resulting tree topology is largely consistent with molecular hypotheses of avian phylogeny. We identify areas that are in broad agreement with current views on avian systematics and also those that require further work. We also highlight the need for leaf-based support measures to enable the identification of rogue taxa in supertrees. This is a first attempt at a supertree of both extinct and extant birds, it is not intended to be utilised in an overhaul of avian systematics or as a basis for taxonomic re-classification but provides a strong basis on which to base further studies on macroevolution, conservation, biodiversity, comparative biology and character evolution, in particular the inclusion of fossils will allow the study of bird evolution and diversification throughout deep time.

Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis.

The hypothesis that patterns of sex-biased dispersal are related to social mating system in mammals and birds has gained widespread acceptance over the past 30 years. However, two major complications have obscured the relationship between these two behaviors: 1) dispersal frequency and dispersal distance, which measure different aspects of the dispersal process, have often been confounded, and 2) the relationship between mating system and sex-biased dispersal in these vertebrate groups has not been examined using modern phylogenetic comparative methods. Here, we present a phylogenetic analysis of the relationship between mating system and sex-biased dispersal in mammals and birds. Results indicate that the evolution of female-biased dispersal in mammals may be more likely on monogamous branches of the phylogeny, and that females may disperse farther than males in socially monogamous mammalian species. However, we found no support for a relationship between social mating system and sex-biased dispersal in birds when the effects of phylogeny are taken into consideration. We caution that although there are larger-scale behavioral differences in mating system and sex-biased dispersal between mammals and birds, mating system and sex-biased dispersal are far from perfectly associated within these taxa.

Promiscuity and the evolutionary transition to complex societies.

Theory predicts that the evolution of cooperative behaviour is favoured by low levels of promiscuity leading to high within-group relatedness. However, in vertebrates, cooperation often occurs between non-relatives and promiscuity rates are among the highest recorded. Here we resolve this apparent inconsistency with a phylogenetic analysis of 267 bird species, demonstrating that cooperative breeding is associated with low promiscuity; that in cooperative species, helping is more common when promiscuity is low; and that intermediate levels of promiscuity favour kin discrimination. Overall, these results suggest that promiscuity is a unifying feature across taxa in explaining transitions to and from cooperative societies.

The supertree tool kit.

BACKGROUND: Large phylogenies are crucial for many areas of biological research. One method of creating such large phylogenies is the supertree method, but creating supertrees containing thousands of taxa, and hence providing a comprehensive phylogeny, requires hundred or even thousands of source input trees. Managing and processing these data in a systematic and error-free manner is challenging and will become even more so as supertrees contain ever increasing numbers of taxa. Protocols for processing input source phylogenies have been proposed to ensure data quality, but no robust software implementations of these protocols as yet exist. FINDINGS: The aim of the Supertree Tool Kit (STK) is to aid in the collection, storage and processing of input source trees for use in supertree analysis. It is therefore invaluable when creating supertrees containing thousands of taxa and hundreds of source trees. The STK is a Perl module with executable scripts to carry out various steps in the processing protocols. In order to aid processing we have added meta-data, via XML, to each tree which contains information such as the bibliographic source information for the tree and how the data were derived, for instance the character data used to carry out the original analysis. These data are essential parts of previously proposed protocols. CONCLUSIONS: The STK is a bioinformatics tool designed to make it easier to process source phylogenies for inclusion in supertree analysis from hundreds or thousands of input source trees, whilst reducing potential errors and enabling easy sharing of such datasets. It has been successfully used to create the largest known supertree to date containing over 5000 taxa from over 700 source phylogenies.

Dinosaurs and the Cretaceous Terrestrial Revolution.

The observed diversity of dinosaurs reached its highest peak during the mid- and Late Cretaceous, the 50 Myr that preceded their extinction, and yet this explosion of dinosaur diversity may be explained largely by sampling bias. It has long been debated whether dinosaurs were part of the Cretaceous Terrestrial Revolution (KTR), from 125-80 Myr ago, when flowering plants, herbivorous and social insects, squamates, birds and mammals all underwent a rapid expansion. Although an apparent explosion of dinosaur diversity occurred in the mid-Cretaceous, coinciding with the emergence of new groups (e.g. neoceratopsians, ankylosaurid ankylosaurs, hadrosaurids and pachycephalosaurs), results from the first quantitative study of diversification applied to a new supertree of dinosaurs show that this apparent burst in dinosaurian diversity in the last 18 Myr of the Cretaceous is a sampling artefact. Indeed, major diversification shifts occurred largely in the first one-third of the group's history. Despite the appearance of new clades of medium to large herbivores and carnivores later in dinosaur history, these new originations do not correspond to significant diversification shifts. Instead, the overall geometry of the Cretaceous part of the dinosaur tree does not depart from the null hypothesis of an equal rates model of lineage branching. Furthermore, we conclude that dinosaurs did not experience a progressive decline at the end of the Cretaceous, nor was their evolution driven directly by the KTR.